Carbon and water flow between plants and the atmosphere is regulated by the opening and closing of minute stomatal pores in surfaces of leaves. By changing the aperture of stomata, plants regulate water loss and photosynthetic carbon gain in response to many environmental stimuli, but stomatal movements cannot yet be reliably predicted. We found that the complexity that characterizes stomatal control in seed plants is absent in early-diverging vascular plant lineages. Lycophyte and fern stomata are shown to lack key responses to abscisic acid and epidermal cell turgor, making their behavior highly predictable. These results indicate that a fundamental transition from passive to active metabolic control of plant water balance occurred after the divergence of ferns about 360 million years ago.